Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T02:35:26.847Z Has data issue: false hasContentIssue false
  • English
  • Français

Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania

Published online by Cambridge University Press:  12 July 2006

V. Y. YURCHENKO ,
J. LUKEš ,
M. JIRKŮ ,
R. ZELEDÓN  and
D. A. MASLOV
V. Y. YURCHENKO
Affiliation:
Albert Einstein College of Medicine of Yeshiva University, Bronx, New York 10461, USA
J. LUKEš
Affiliation:
Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and Faculty of Biology, University of South Bohemia, ̆Ceské Budějovice (Budweis) 37005, Czech Republic
M. JIRKŮ
Affiliation:
Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and Faculty of Biology, University of South Bohemia, ̆Ceské Budějovice (Budweis) 37005, Czech Republic
R. ZELEDÓN
Affiliation:
School of Veterinary Medicine, National University, Heredia, Costa Rica
D. A. MASLOV
Affiliation:
Department of Biology, University of California – Riverside, Riverside, California 92521, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

A flagellate isolated from the intestinal tract of a reduviid bug Ricolla simillima (Heteroptera) in Costa Rica was found to represent a new trypanosomatid species by the phylogenetic analysis of small subunit ribosomal RNA (SSU rRNA), glyceraldehyde phosphate dehydrogenase (GAPDH) and large subunit of RNA polymerase II (RPOIILS) genes. The phylogenetic position of this trypanosomatid, together with its typical promastigote morphology and the host identity, allowed its classification as a species that belongs to the polyphyletic genus Leptomonas. Interestingly, the new species was revealed as a member of the novel phylogenetic clade representing the closest known relative of Leishmania. With the new species used as an outgroup to root the Leishmania RPOIILS phylogenetic tree, the lineage of the Neotropical species L. enriettii was found to branch off early, and was followed by a deep split between the Old World and the remaining New World species. This tree topology supports the hypothesis that the initial transition to dixenous parasitism in this group pre-dated the continental split and that afterwards the Neotropical and the Old World groups evolved largely independently.

Keywords

Leptomonas costaricensisphylogenyTrypanosomatidaeLeishmaniaevolution of parasitismdixenous parasitism
Type
Research Article
Information
Parasitology , Volume 133 , Issue 5 , November 2006 , pp. 537 - 546
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Boisseau-Garsaud, A. M., Cales-Quist, D., Desbois, N., Jouannelle, J., Jouannelle, A., Pratlong, F. and Dedet, J. P. ( 2000). A new case of cutaneous infection by a presumed monoxenous trypanosomatid in the island of Martinique (French West Indies). Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 51–52.CrossRefGoogle Scholar
Carvalho, A. L. M. and Deane, M. P. ( 1974). Trypanosomatids isolated from Zelus leucogrammus (Perty, 1834) (Hemiptera, Reduviidae), with a discussion on flagellates of insectivorous bugs. Journal of Protozoology 21, 5–8.CrossRefGoogle Scholar
Croan, D. and Ellis, J. ( 1996). Phylogenetic relationships between Leishmania, Viannia and Sauroleishmania inferred from comparison of a variable domain within the RNA polymerase II largest subunit gene. Molecular and Biochemical Parasitology 79, 97–102.CrossRefGoogle Scholar
Croan, D. G., Morrison, D. A. and Ellis, J. T. ( 1997). Evolution of the genus Leishmania revealed by comparison of DNA and RNA polymerase gene sequences. Molecular and Biochemical Parasitology 89, 149–159.CrossRefGoogle Scholar
Cupolillo, E., Medina-Acosta, E., Noyes, H., Momen, H. and Grimaldi, G., Jr ( 2000). A revised classification for Leishmania and Endotrypanum. Parasitology Today 16, 142–144.CrossRefGoogle Scholar
Fernandes, A. P., Nelson, K. and Beverley, S. M. ( 1993). Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: Perspectives on the age and origins of parasitism. Proceedings of the National Academy of Sciences, USA 90, 11608–11612.CrossRefGoogle Scholar
Galtier, N., Gouy, M. and Gautier, C. ( 1996). SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences 12, 543–548.CrossRefGoogle Scholar
Garin, Y. J. F., Sulahian, A., Méneceur, P., Pratlong, F., Prina, E., Gangneux, J. P., Dedet, J. P. and Derouin, F. ( 2001). Experimental pathogenicity of a presumed monoxenous trypanosomatid isolated from humans in a murine model. Journal of Eukaryotic Microbiology 48, 170–176.CrossRefGoogle Scholar
Hoare, C. A. and Wallace, F. G. ( 1966). Developmental stages of trypanosomatid flagellates: a new terminology. Nature, London 212, 1385–1386.CrossRefGoogle Scholar
Hollar, L., Lukeš, J. and Maslov, D. A. ( 1998). Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. Journal of Eukaryotic Microbiology 45, 293–297.CrossRefGoogle Scholar
Kerr, S. F. ( 2000). Palaearctic origin of Leishmania. Memórias do Instituto Oswaldo Cruz 95, 75–80.CrossRefGoogle Scholar
Kerr, S. F., Merkelz, R. and Mackinnon, C. ( 2000). Further support for a Palaearctic origin of Leishmania. Memórias do Instituto Oswaldo Cruz 95, 579–581.CrossRefGoogle Scholar
Lainson, R. ( 1997). On Leishmania enriettii and other enigmatic Leishmania species of the Neotropics. Memórias do Instituto Oswaldo Cruz 92, 377–387.CrossRefGoogle Scholar
Lainson, R. and Shaw, J. J. ( 1987). Evolution, classification and geographical distribution. In The Leishmaniases in Biology and Medicine ( ed. Peters, W. and Killick-Kendrick, R.), pp. 1–120. Academic Press, London.
Maslov, D. A., Lukeš, J., Jirků, M. and Simpson, L. ( 1996). Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Molecular and Biochemical Parasitology 75, 197–205.CrossRefGoogle Scholar
Maslov, D. A. and Simpson, L. ( 1995). Evolution of parasitism in kinetoplastid protozoa. Parasitology Today 11, 30–32.CrossRefGoogle Scholar
Merzlyak, E., Yurchenko, V., Kolesnikov, A. A., Alexandrov, K., Podlipaev, S. A. and Maslov, D. A. ( 2001). Diversity and phylogeny of insect trypanosomatids based on small subunit rRNA genes: Polyphyly of Leptomonas and Blastocrithidia. Journal of Eukaryotic Microbiology 48, 161–169.CrossRefGoogle Scholar
Momen, H. and Cupolillo, E. ( 2000). Speculations on the origin and evolution of the genus Leishmania. Memórias do Instituto Oswaldo Cruz 95, 583–588.CrossRefGoogle Scholar
Noyes, H. ( 1998). Implications of a Neotropical origin of the genus Leishmania. Memórias do Instituto Oswaldo Cruz 93, 657–662.CrossRefGoogle Scholar
Noyes, H. A., Arana, B. A., Chance, M. L. and Maingon, R. ( 1997). The Leishmania hertigi (Kinetoplastida; Trypanosomatidae) complex and the lizard Leishmania: their classification and evidence for a neotropical origin of the Leishmania-Endotrypanum clade. Journal of Eukaryotic Microbiology 44, 511–517.CrossRefGoogle Scholar
Noyes, H. A., Camps, A. P. and Chance, M. L. ( 1996). Leishmania herreri (Kinetoplastida; Trypanosomatidae) is more closely related to Endotrypanum (Kinetoplastida; Trypanosomatidae) than to Leishmania. Molecular and Biochemical Parasitology 80, 119–123.CrossRefGoogle Scholar
Noyes, H., Pratlong, F., Chance, M., Ellis, J., Lanotte, G. and Dedet, J. P. ( 2002). A previously unclassified trypanosomatid responsible for human cutaneous lesions in Martinique (French West Indies) is the most divergent member of the genus Leishmania ss. Parasitology 124, 17–24.CrossRefGoogle Scholar
Philippe, H. ( 1998). Molecular phylogeny of kinetoplastids. In Evolutionary Relationships among Protozoa ( ed. Coombs, G. H., Vickerman, K., Sleigh, M. A. and Warren, A.), pp. 195–212. Kluwer Academic Publishers, Dordrecht, Boston, London.
Podlipaev, S. A. ( 2003). Host specificity of homoxenous trypanosomatids. Parasitologia (In Russian) 37, 3–17.Google Scholar
Posada, D. and Crandall, K. A. ( 1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
Pratlong, F., Dereure, J., Bucheton, B., El-Saf, S., Dessein, A., Lanotte, G. and Dedet, J. P. ( 2001). Sudan: the possible original focus of visceral leishmaniasis. Parasitology 122, 599–605.CrossRefGoogle Scholar
Simpson, A. G. B., Stevens, J. R. and Lukeš, J. ( 2006). The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology 22, 168–174.CrossRefGoogle Scholar
Stevens, J. R. and Gibson, W. C. ( 1999). The molecular evolution of trypanosomes. Parasitology Today 15, 432–437.CrossRefGoogle Scholar
Stevens, J. R., Noyes, H. A., Dover, G. A. and Gibson, W. C. ( 1999). The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.CrossRefGoogle Scholar
Swofford, D. L. ( 1998). PAUP* 4.0: Phylogenetic Analysis Using Parsimony (and Other Methods), Beta Version, 1998. Sinauer Associates, Inc., Sunderland, MA.
Thomaz-Soccol, V., Pratlong, F., Langue, R., Castro, E., Luz, E. and Dedet, J. P. ( 1996). New isolation of Leishmania enriettii Muniz and Medina, 1948 in Paraná state, Brazil, 50 years after the first description, and isoenzymatic polymorphism of the L. enriettii taxon. Annals of Tropical Medicine and Parasitology 90, 491–495.CrossRefGoogle Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. ( 1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
Vickerman, K. ( 1976). The diversity of the kinetoplastid flagellates. In Biology of the Kinetoplastida ( ed. Lumsden, W. H. R. and Evans, D. A.), pp. 1–34. Academic Press, London, New York, San Francisco.
Vickerman, K. ( 1994). The evolutionary expansion of the trypanosomatid flagellates. International Journal for Parasitology 24, 1317–1331.CrossRefGoogle Scholar
Wallace, F. G. ( 1966). The trypanosomatid parasites of insects and arachnids. Experimental Parasitology 18, 124–193.CrossRefGoogle Scholar
Westenberger, S. J., Sturm, N. R., Yanega, D., Podlipaev, S. A., Zeledón, R., Campbell, D. A. and Maslov, D. A. ( 2004). Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the Spliced Leader RNA gene. Parasitology 129, 537–547.CrossRefGoogle Scholar
Yurchenko, V., Lukeš, J., Xu, X. and Maslov, D. A. ( 2006). An integrated morphological and molecular approach to a new species description in the Trypanosomatidae: the case of Leptomonas podlipaevi n. sp., a parasite of Boisea rubrolineata (Hemiptera: Rhopalidae). Journal of Eukaryotic Microbiology 53, 103–111.Google Scholar